Wagman et al. Malar J (2018) 17:19 https://doi.org/10.1186/s12936-017-2168-2 Malaria Journal RESEARCH Open Access An observational analysis of the impact of indoor residual spraying with non‑pyrethroid insecticides on the incidence of malaria in Ségou Region, Mali: 2012–2015 Joseph Wagman1*, Christelle Gogue1, Kenzie Tynuv1, Jules Mihigo2, Elie Bankineza3, Mamadou Bah3, Diadier Diallo4, Andrew Saibu5, Jason H. Richardson6, Diakalkia Kone7, Seydou Fomba7, Jef Bernson8, Richard Steketee9, Laurence Slutsker9 and Molly Robertson1 Abstract Background: Ségou Region in Central Mali is an area of high malaria burden with seasonal transmission, high access to and use of long-lasting insecticidal nets (LLINs), and resistance to pyrethroids and DDT well documented in Anoph- eles gambiae s.l. (the principal vector of malaria in Mali). Ségou has recently received indoor residual spraying (IRS) sup- ported by Mali’s collaboration with the US President’s Malaria Initiative/Africa Indoor Residual Spraying programme. From 2012 to 2015, two diferent non-pyrethroid insecticides: bendiocarb in 2012 and 2013 and pirimiphos-methyl in 2014 and 2015, were used for IRS in two districts. This report summarizes the results of observational analyses carried out to assess the impact of these IRS campaigns on malaria incidence rates reported through local and district health systems before and after spraying. Methods: A series of retrospective time series analyses were performed on 1,382,202 rapid diagnostic test-confrmed cases of malaria reported by district routine health systems in Ségou Region from January 2012 to January 2016. Malaria testing, treatment, surveillance and reporting activities remained consistent across districts and years dur- ing the study period, as did LLIN access and use estimates as well as An. gambiae s.l. insecticide resistance patterns. Districts were stratifed by IRS implementation status and all-age monthly incidence rates were calculated and com- pared across strata from 2012 to 2014. In 2015 a regional but variable scale-up of seasonal malaria chemoprevention complicated the region-wide analysis; however IRS operations were suspended in Bla District that year so a diference in diferences approach was used to compare 2014 to 2015 changes in malaria incidence at the health facility level in children under 5-years-old from Bla relative to changes observed in Barouéli, where IRS operations were consistent. Results: During 2012–2014, rapid reductions in malaria incidence were observed during the 6 months following each IRS campaign, though most of the reduction in cases (70% of the total) was concentrated in the frst 2 months after each campaign was completed. Compared to non-IRS districts, in which normal seasonal patterns of malaria incidence were observed, an estimated 286,745 total fewer cases of all-age malaria were observed in IRS districts. The total cost of IRS in Ségou was around 9.68 million USD, or roughly 33.75 USD per case averted. Further analysis sug- gests that the timing of the 2012–2014 IRS campaigns (spraying in July and August) was well positioned to maximize public health impact. Suspension of IRS in Bla District after the 2014 campaign resulted in a 70% increase in under-5- years-old malaria incidence rates from 2014 to 2015, signifcantly greater (p 0.0003) than the change reported from Barouéli District, where incidence rates remained the same. = *Correspondence: [email protected] 1 PATH, Washington, DC, USA Full list of author information is available at the end of the article © The Author(s) 2018. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/ publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Wagman et al. Malar J (2018) 17:19 Page 2 of 15 Conclusions: From 2012 to 2015, the annual IRS campaigns in Ségou are associated with several hundred thousand fewer cases of malaria. This work supports the growing evidence that shows that IRS with non-pyrethroid insecti- cides is a wise public health investment in areas with documented pyrethroid resistance, high rates of LLIN coverage, and where house structures and population densities are appropriate. Additionally, this work highlights the utility of quality-assured and validated routine surveillance and well defned observational analyses to rapidly assess the impact of malaria control interventions in operational settings, helping to empower evidence-based decision making and to further grow the evidence base needed to better understand when and where to utilize new vector control tools as they become available. Keywords: Indoor residual spraying, Malaria incidence, Observational analysis, Mali, Next generation IRS Background Despite this need, widespread adoption of new prod- Over the past 15 years global eforts to control and pre- ucts for IRS is hampered by several complex factors vent malaria have produced some astounding results. among which are concerns about increased costs as well Estimates indicate that between 2000 and 2015 world- as gaps that exist in the evidence base needed to evaluate wide malaria incidence has declined almost 40% in areas the impact of newer products in various malaria trans- at risk (from 146 cases per 1000 people per annum to 91 mission settings and in combination with other malaria cases per 1000 people per annum) and malaria mortality control interventions. Nonetheless, there are a few cur- rates have decreased by almost 60% in areas at risk (from rently available pyrethroid alternatives recommended by 47 deaths per 100,000 people per annum to 19 deaths WHO for IRS targeting malaria vectors. Two of the most per 100,000 people per annum) [1]. Tis is refective of widely available products include a wettable powder worldwide progress in malaria that has come about, (WP) formulation of bendiocarb, a carbamate insecticide, in part, through implementation of a package of stand- and a micro-encapsulated formulation of pirimiphos- ard evidence-based interventions of which malaria vec- methyl (PM CS), an organophosphate insecticide [11], tor control has been a central component [1, 2]. Indeed, both of which have been used by the US President’s Bhat and others recently estimated that 81% of all malaria Malaria Initiative (PMI) Africa Indoor Residual Spraying cases averted from 2000 to 2015 could be attributed to (AIRS) Project in recent years [12, 13]. While the insec- successful vector control interventions, namely the large- ticidal efcacy of bendiocarb has been well established scale distribution and use of insecticide-treated nets experimentally [14, 15], and there are indications that (including long-lasting insecticidal nets, or LLINs) and it can have a positive impact in reducing malaria trans- the indoor residual spraying (IRS) of insecticides inside mission in areas with pyrethroid-resistant mosquitoes homes [3]. Even in Mali, where malaria control eforts are [16–19], signifcant concerns about poor residual efcacy challenged by complex and intense transmission cycles [20–22] and emerging resistance [23, 24] have recently as well as political instability, IRS and LLINs are thought led to a shift in PMI/AIRS operations away from spray- to have contributed (along with improved malaria case ing bendiocarb and towards the use of PM, both through- management) to decreasing trends in all cause child mor- out Africa in general [12] and in Mali specifcally [25]. tality observed over the last 10 years [2, 4, 5]. However, wider-spread adoption and scale-up of PM has While vector control is recognized as an integral part been hampered by its higher cost. To help meet this chal- of the present and future global malaria control and elim- lenge, the Next Generation IRS (NgenIRS) project has ination efort [6–8], the continued success of currently introduced a co-payment mechanism for PM as part of available tools is threatened by the rapid emergence and a broad market-shaping efort for third generation IRS spread of insecticide resistance in key mosquito popula- (3GIRS) products that includes wide-ranging impact tions [9, 10]. Particularly worrisome is resistance to pyre- analyses. By defnition, a 3GIRS product is one that is throids, the most commonly used class of insecticide designed to be efective against pyrethroid-resistant mos- for malaria vector control (and currently the only class quitoes and have an indoor residual efcacy of at least available on LLINs), which is now widespread and found 6 months. throughout most of sub-Saharan Africa [1]. Accord- Here, an observational, retrospective (2012–2015) ingly, WHO and others have recognized an urgent need time-series analysis of the seasonal epidemiological to develop next-generation, non-pyrethroid insecticide impact of IRS with bendiocarb WP and PM CS in the products in order to preserve our ability to utilize IRS Ségou Region (Ségou) of central Mali is presented to: (1) and LLINs for malaria prevention [2, 10]. help further expand the evidence base needed to evalu- ate the public health impact and cost efectiveness of IRS Wagman et al. Malar J (2018) 17:19 Page 3 of 15 campaigns utilizing non-pyrethroid, including 3GIRS pyrethroids and DDT but susceptible to carbamates and products; and (2) help foster the use of quality-assured organophosphates [28, 31], and a gradual scale-up of and validated routine malaria surveillance data for evi- seasonal malaria chemoprevention (SMC) that began in dence-based decision making. 2013 [4]. Importantly, Ségou also contains two districts, Bla and Barouéli, selected to participate in the PMI/AIRS Methods Project during this time, having been sprayed with ben- Study site and malaria landscape diocarb WP in 2012 and 2013 and PM CS in 2014.
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